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JOURNAL ARTICLES
Alterations in somite patterning of Myf-5-deficient mice: a possible role for FGF-4 and FGF-6
S. Grass, H.H. Arnold, T. Braun
Development 1996 122: 141-150;

Summary

Mice carrying a targeted mutation in the gene for the myogenic factor Myf-5 fail to form major parts of the ribs, which leads to an unstable thorax and perinatal death. Here, we report that somites of Myf-5-deficient mice lack the expression of FGF-4 and FGF-6 while TGF beta-2 is expressed normally. Early sclerotomal markers, such as Pax-1 reveal no substantial reduction of sclerotome size. At E11.5 the condensing mesenchyme of the rib anlagen is considerably reduced in size in Myf-5 mutant mice. This may be caused by the lack of Myf-5-positive, FGF-expressing cells which normally are in close contact with the lateral sclerotome generating the rib progenitors. The potential role of FGFs and TGF beta on sclerotome formation is demonstrated in micromass cultures of early somites. Combinations of FGF-4 or FGF-6 with TGF beta-2 potentiate chondrogenesis suggesting that these growth factors emanating from early myotomal and dermomyotomal cells may have instructive or permissive effects on differentiation or outgrowth of sclerotomal cells.

Reference

    1. Bober E.,
    2. Lyons G. E.,
    3. Braun T.,
    4. Cossu G.,
    5. Buckingham M.,
    6. Arnold H. H.
    (1991) The muscle regulatory gene, myf6, has a biphasic pattern of expression during early mouse development. J. Cell Biol 113, 1255–1265
    OpenUrlAbstract/FREE Full Text
    1. Bober E.,
    2. Franz T.,
    3. Arnold H.-H.,
    4. Gruss P.,
    5. Tremblay P.
    (1994) Pax-3 is required for the development of limb muscles: a possible role for the migration of dermomyotomal muscle progenitor cells. Development 120, 603–612
    OpenUrlAbstract
    1. Braun T.,
    2. Rudnicki M. A.,
    3. Arnold H.-H.,
    4. Jaenisch R.
    (1992) Targeted inactivation of the muscle regulatory gene Myf-5 results in abnormal rib development and perinatal death. Cell 71, 369–382
    OpenUrlCrossRefPubMedWeb of Science
    1. Braun T.,
    2. Arnold H.-H.
    (1994) ES-cells carrying two inactivated Myf-5 alleles form skeletal muscle cells: Activation of an alternative Myf-5-independent differentiation pathway. Dev. Biol 164, 24–36
    OpenUrlCrossRefPubMedWeb of Science
    1. Braun T.,
    2. Bober E.,
    3. Rudnicki M. A.,
    4. Jaenisch R.,
    5. Arnold H. H.
    (1994) MyoD expression marks the onset of skeletal myogenesis in Myf-5 mutant mice. Development 120, 3083–3092
    OpenUrlAbstract
    1. Braun T.,
    2. Arnold H.-H.
    (1995) Inactivation of Myf-6 and Myf-5 genes in mice leads to alterations in skeletal development. EMBO J 14, 1176–1186
    OpenUrlPubMedWeb of Science
    1. Centrella M.,
    2. Horowitz M. C.,
    3. Wozney J. M.,
    4. McCarthey T. L.
    (1994) Transforming growth factor-gene family and bone. Endocrine Rev 15, 27–39
    OpenUrlCrossRefPubMedWeb of Science
    1. Christ B.,
    2. Jacob H.,
    3. Jacob B.
    (1978) On the formation of the myotoms in avian embryos. An experimental and scanning electron microscope study. Experientia 34, 514–516
    OpenUrlCrossRef
    1. Christ B.,
    2. Brand-Saberi B.,
    3. Grim M.,
    4. Wilting J.
    (1992) Local signalling in dermomyotomal cell type specification. Anat. Embryol 186, 505–510
    OpenUrlPubMed
    1. Clare J. J.,
    2. Rayment F. B.,
    3. Ballantine S. P.,
    4. Sreekrishna K.,
    5. Romanos M. A.
    (1991) High level expression of tetanus toxin fragment C in Pichia Pastoris strains containing multiple tandem integrations of the gene. Biotechnology 9, 455–460
    OpenUrlCrossRefPubMed
    1. Deutsch U.,
    2. Dressler G.,
    3. Gruss P.
    (1988) Pax1 a member of the paired box homologous murine gene family, is expressed in segmented structures during development. Cell 53, 617–625
    OpenUrlCrossRefPubMedWeb of Science
    1. Dickson M. C.,
    2. Slager H. G.,
    3. Duffie E.,
    4. Mummery C. L.,
    5. Akhurst R. J.
    (1993) RNA and protein localization of TGF2 in the early mouse embryo suggest an involvement in cardiac development. Development 117, 625–639
    OpenUrlAbstract
    1. Erlebacher A.,
    2. Filvaroff E. H.,
    3. Gitelman S. E.,
    4. Derynck R.
    (1995) Towards a molecular understanding of skeletal development. Cell 80, 371–378
    OpenUrlCrossRefPubMedWeb of Science
    1. Fan C.-M.,
    2. Tessier-Lavigne M.
    (1994) Patterning of mammalian somites by surface ectoderm and notochord: evidence for sclerotome induction by a hedgehog homologue. Cell 79, 1175–1186
    OpenUrlCrossRefPubMedWeb of Science
    1. Feldman B.,
    2. Poueymirou W.,
    3. Papaioannou V. E.,
    4. DeChiaria T. M.,
    5. Goldfarb M.
    (1995) Requirement of FGF-4 for postimplantation mouse development. Science 267, 246–249
    OpenUrlAbstract/FREE Full Text
    1. Frenz D. A.,
    2. Liu W.,
    3. Williams J. D.,
    4. Hatcher V.,
    5. Galinovic-Schwartz V.,
    6. Flanders K. C.,
    7. Van De Water T. R.
    (1994) Induction of chondrogenesis: requirement for synergistic interaction of basic fibroblast growth factor and transforming growth factor-beta. Development 120, 415–424
    OpenUrlAbstract
    1. Globus R. K.,
    2. Patterson-Buckendahl P.,
    3. Gospodarowicz D.
    (1988) Regulation of bovine cell proliferation by fibroblast growth factor and transforming growth factor. Endocrinology 123, 98–105
    OpenUrlCrossRefPubMedWeb of Science
    1. Goldfarb M.
    (1990) The fibroblast growth factor family. Cell Growth Diff 1, 439–445
    OpenUrlPubMedWeb of Science
    1. Goldhammer D. J.,
    2. Brunk B. P.,
    3. Faerman A.,
    4. King A.,
    5. Shani M.,
    6. Emerson C. P., Jr
    (1995) Embryonic activation of the myoD gene is regulated by a highly conserved distal control element. Development 121, 637–649
    OpenUrlAbstract
    1. Hebert J. M.,
    2. Rosenquist T.,
    3. Götz J.,
    4. Martin G. R.
    (1994) FGF-5 as a regulator of the hair growth cycle: evidence from targeted and spontanteous mutations. Cell 78, 1017–1025
    OpenUrlCrossRefPubMedWeb of Science
    1. Hebrok M.,
    2. Wertz K.,
    3. Fuchtbauer E.-M.
    (1994) M-twist is an inhibitor of muscle differentiation. Devel. Biol 165, 537–544
    OpenUrlCrossRefPubMedWeb of Science
    1. Huang R.,
    2. Zhi Q.,
    3. Christ B.
    (1994) The fate of somitocoele cells in avian embryos. Anat. Embryol 190, 243–250
    OpenUrlPubMed
    1. Johnson R. L.,
    2. Laufer E.,
    3. Riddle R. D.,
    4. Tabin C.
    (1994) Ectopic expression of sonic hedgehog alters dorsal-ventral patterning of somites. Cell 79, 1165–1173
    OpenUrlCrossRefPubMedWeb of Science
    1. Keynes R.,
    2. Stern C.
    (1988) Mechanisms of vertebrate segmentation. Development 103, 413–429
    OpenUrlPubMedWeb of Science
    1. Kimelman D.,
    2. Kirschner N.
    (1987) Synergistic induction of mesoderm by FGF and TGF-and the identification of FGF in the early embryo. Cell 51, 869–871
    OpenUrlCrossRefPubMedWeb of Science
    1. Kingsley D. M.,
    2. Bland A. E.,
    3. Grubber J. M.,
    4. Marker P. C.,
    5. Russell L. B.,
    6. Copeland N. G.,
    7. Jenkins N. A.
    (1992) The mouse short ear skeletal morphogenesis locus is associated with defects in a bone morphogenetic member of the TGFsuperfamily. Cell 71, 399–410
    OpenUrlCrossRefPubMedWeb of Science
    1. Kulyk W. H.,
    2. Rodgers B. J.,
    3. Greer K.,
    4. Kosher R. A.
    (1989) Promotion of embryonic limb cartilage differentiation by Transforming Growth Factor-. Dev. Biol 135, 424–430
    OpenUrlCrossRefPubMedWeb of Science
    1. Lefebvre P. P.,
    2. Staecker H.,
    3. Weber T.,
    4. Van De Water T. R.,
    5. Moonen G.
    (1991) TGF-1 modulates bFGF receptor message expression in cultured adult mouse auditory neurons. NeuroReport 2, 305–308
    OpenUrlPubMedWeb of Science
    1. deLapeyriere O.,
    2. Ollendorff V.,
    3. Planche J.,
    4. Ott M.O.,
    5. Pizette S.,
    6. Coulier F.,
    7. Birnbaum D.
    (1993) Expression of the FGF6 gene is restricted to developing skeletal muscle in the mouse embryo. Development 118, 601–611
    OpenUrlAbstract
    1. Lotan R.,
    2. Skutelsky E.,
    3. Danon D.,
    4. Sharon N.
    (1975) The purification, composition and specificity of the anti-T lectin from peanut (Arachis hypogaea). J. Biol. Chem 250, 8518–8523
    OpenUrlAbstract/FREE Full Text
    1. Massague J.
    (1987) The TGF-family of growth and differentiation factors. Cell 49, 437–438
    OpenUrlCrossRefPubMedWeb of Science
    1. Niswander L.,
    2. Martin G. R.
    (1992) FGF-4 expression during gastrulation, myogenesis, limb and tooth development in the mouse. Development 114, 755–768
    OpenUrlAbstract
    1. Niswander L.,
    2. Tickle C.,
    3. Vogel A.,
    4. Booth I.,
    5. Martin G. R.
    (1993) FGF-4 replaces the apical ectodermal ridge and directs outgrowth and patterning of the limb. Cell 75, 579–587
    OpenUrlCrossRefPubMedWeb of Science
    1. Olson E. N.,
    2. Klein W. H.
    (1994) bHLH factors in muscle development: dead lines and commitments, what to leave in and what to leave out. Genes Dev 8, 1–8
    OpenUrlFREE Full Text
    1. Porquie O.,
    2. Coltey M.,
    3. Teillet M.-A.,
    4. Ohrdahl C.,
    5. LeDouarin N. M.
    (1993) Control of dorsoventral patterning of somitic derivatives by notochord and floor plate. Proc. Natl. Acad. Sci. USA 90, 5242–5246
    OpenUrlAbstract/FREE Full Text
    1. Reardon W.,
    2. Winter R. M.,
    3. Rutland P.,
    4. Pulleyn L. J.,
    5. Jones B. M.,
    6. Malcolm S.
    (1994) Mutations in the fibroblast growth factor receptor 2 gene causes Crouzon syndrome. Nature Genet 8, 98–103
    OpenUrlCrossRefPubMedWeb of Science
    1. Rousseau F.,
    2. Bonaventure J.,
    3. Legeai-Mallet L.,
    4. Pelet A.,
    5. Rozet J. M.,
    6. Maroteaux P.,
    7. Le Merrer M.,
    8. Munnich A.
    (1994) Mutations in the gene encoding fibroblast growth factor receptor-3 in achondroplasia. Nature 371, 252–254
    OpenUrlCrossRefPubMedWeb of Science
    1. Rousseau F.,
    2. Saugier P.,
    3. Le Merrer M.,
    4. Munnich A.,
    5. Delezoide A.-L.,
    6. Maroteaux P.,
    7. Bonaventure J.,
    8. Narcy F.,
    9. Sanak M.
    (1995) Stop codon FGFR3 mutations in thanatophoric dwarfism type 1. NatureGenet 10, 11–12
    OpenUrlCrossRefPubMedWeb of Science
    1. Shiang R.,
    2. Thompson L. M.,
    3. Zhu Y. Z.,
    4. Church D. M.,
    5. Fielder T. J.,
    6. Bocian M.,
    7. Winokur S. T.,
    8. Wasmuth J. J.
    (1994) Mutations in thetransmembrane domain of FGFR3 cause the most common genetic form of dwarfism, achondroplasia. Cell 78, 335–342
    OpenUrlCrossRefPubMedWeb of Science
    1. Storm E. E.,
    2. Huynh T. V.,
    3. Copeland N. G.,
    4. Jenkins N. A.,
    5. Kingsley D. M.,
    6. Lee S. J.
    (1994) Limb alterations in brachypodism mice due to mutations in a new member of the TGF-superfamily. Nature 368, 639–643
    OpenUrlCrossRefPubMedWeb of Science
    1. Tajbakhsh S.,
    2. Buckingham M.
    (1994) Mouse limb muscle isdetermined in the absence of the earliest myogenic factor myf-5. Proc. Natl. Acad. Sci. USA 91, 747–751
    OpenUrlAbstract/FREE Full Text
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JOURNAL ARTICLES
Alterations in somite patterning of Myf-5-deficient mice: a possible role for FGF-4 and FGF-6
S. Grass, H.H. Arnold, T. Braun
Development 1996 122: 141-150;
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